It was designed by Denton Corker Marshall Architects and finished construction in 2001. Situated in the Carlton Gardens, it was commissioned by the Victorian Government Office of Major Projects on behalf of Museums Victoria. The museum is a rich response to Melbourne’s urban condition, and provides a place for education, history, culture and society to engage with each other in a contemporary setting. It is now an important part of Melbourne’s soft infrastructure.

The museum has seven main galleries, a Children's Gallery and a temporary exhibit gallery on three levels, Upper, Ground and Lower Level and was constructed by Baulderstone Hornibrook.

The Touring Hall is where temporary exhibits are displayed. Past exhibits include mummies from Egypt and dinosaurs from China. The Big Box is part of the Children's Gallery.

In addition, the museum has other facilities such as the Sidney Myer Amphitheatre and The Age Theatre. The Discovery Centre, on the Lower Level, is a free public research centre. The museum also has a cafe and a souvenir shop.

The IMAX Theatre, which is situated on the Lower Level is also part of the museum complex. It shows movies, usually documentary films, in 3-D format.

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The Melbourne Museum is a post-modernist building, structured with a grid-like order that embraces eccentric metal clad forms extruding out and creating an irregular sculptural composition with moments of abstract colour throughout the building. A building of the public, the museum is arranged in a volumetrically individual layout, referencing Melbourne’s iconic Hoddle Grid, which allows the importance of each component of the buildings historical, cultural and social significance to be read in loosely equal hierarchy and individuality, being the Imax theatre, and Aboriginal centre.[1] The building is can be dissected into different spaces so an individual can navigate through and around the building in an orthogonal manner. It is both a single building, and a network of individual buildings integrated into the landscape of the Carlton Gardens. The new museum is axially aligned with the adjacent neo-classical Royal Exhibition Building, and references it along with the skyscrapers of Melbourne’s central business district, with its monumental scale, and horizontality with protruding vertical facets. The sticks and blades that make up the Melbourne Museum are signatures of Denton Corker Marshall’s architecture. The most iconic detail of the building is the spectacular cantilever that projects over to the west, on the central axis with the Royal Exhibition centre, this cantilever can be seen from kilometres away. On the northern side resides a large, taller sloped roof than that of the cantilever, similar in scale to the dome of the Royal Exhibition building.

Denton Corker Marshall specialise in city planning and urban design, and mainly concern their practise with responding to social desires. The Melbourne Museum is situated in a unique precinct; adjacent to a large local landmark, located within a large public park. Contrasted against the neo-classical Royal Exhibition centre, Denton Corker Marshall separates the two with an events plaza, yet connects them again underground with a car park, defining their motto; "A new connection between the old, the new, past and future".[2] Their approach to such a prominent part of Melbourne’s historical and cultural infrastructure was to bring the past and existing exhibition building, into a new context and attempting to redefine a museums role as a public building.[3] Denton Corker Marshall also envision the building to be just as responsive to its context as it is now, in the future. In a meeting place for community, the building itself acts as a community of different programs and meanings, combining to make a whole. In a wider context, the museum refers to Melbourne’s city grid in its planning, and integrates the landscape of Carlton Gardens; housing a Forest Gallery which is situated within the building, and also providing areas of exterior circulation around the building. Formally the Melbourne Museum is motivated by sculpture. Denton Corker Marshall manipulates sculptural forms to meet the constraints of the buildings context and program.[4]

Melbourne Museum was originally located (along with the State Library and the old state gallery) in the city block between La Trobe, Swanston, Little Lonsdale and Russell Streets - the nearby Museum underground railway station was originally named after it, although following the move the station was renamed Melbourne Central. The State Library now uses all the space in that building, the gallery also having moved to the NGV site in St Kilda Road.

The period in which the Victorian government was led by the Premier Sir Rupert Hamer (1972 - 1981) was one of policy development for museums in Victoria. Hamer's Arts Minister the Hon. Norman Lacy established a Museums Development Committee[3] consisting of representatives of the Science Museum of Victoria, the National Museum of Victoria and the Ministry for the Arts. It considered such matters as the development of a single City Museum complex leading eventually to the establishment of the new Melbourne Museum in Carlton and programs in fields such as social history. The Committee also joined with a working party of the Victorian Council of the Arts to develop a comprehensive museums policy for Victoria. Lacy also began the establishment of the Heide Museum of Modern Art with the acquisition of the property Heide II (in Bulleen east of Melbourne) and a collection of 113 art works from John and Sunday Reed in August 1980. It was officially opened in November 1981. He also developed a proposal for a Museum of Social and Political History[4] at the Old Treasury Building for the Executive Committee of Victoria's 150th Anniversary Celebrations in July 1981 which led to the establishment of the City Museum.

The new Melbourne Museum is located on the site of the former Melbourne Exhibition Speedway which operated from 5 November 1928 until 7 March 1936. The 413 yards (378 metres) dirt track speedway took place on a track laid out on the former sports oval and generally catered to motorcycle Solo and Sidecar racing and is considered to be the birthplace of Sidecar speedway racing. The inaugural Australian Sidecar Speedway Championship was staged there in 1931 and was won by Victorians Les Medlycott and "Tich" Jones. The Exhibition Speedway also hosted the Victorian Solo Championship from 1928/29 until 1934/35.

Mind and Body Gallery - a gallery regarding the human body. It also features a world first exhibition about the mind called 'Mind: enter the labyrinth'.

Evolution Gallery - the upper level features the exhibition 'Darwin to DNA'.

Forest Gallery - a living temperate Victorian forest environment, complete with live birds, reptiles, and other fauna

Bunjilaka Aboriginal Cultural Centre - including galleries with exhibitions by and about the Aboriginal peoples of Victoria

Te Pasifika Gallery - an exhibition which highlights the history and watercrafts of Pacific Islanders

Children's Gallery - exhibitions aimed at 3 to 8 year olds.

Touring Hall - is where international touring exhibitions are displayed. 'A Day In Pompeii' which was on display at Melbourne Museum from 26 June to 25 October 2009 was Melbourne Museum's most popular temporary exhibition. Past Touring Hall exhibitions include 'Hatching the Past: Dinosaur Eggs and Babies' (30 May 2008 to 24 August 2008), 'The Great Wall of China: Dynasties, dragons and warriors' (23 March 2007 to 22 July 2007), 'Spirit of the Games: the Opening Ceremony revealed' (18 March to 23 July 2006) and 'Dinosaurs from China' (2005).

Public spaces - Outside the main galleries are various displays relating to Victoria's and Australia's history, including CSIRAC (an early computer built in Australia) and a Pygmy Blue Whale.

Melbourne Museum was one of the venues of Festival Melbourne 2006, a city-wide art festival held in conjunction of the 2006 Commonwealth Games, which was held in Melbourne. Among the exhibitions held in the museum were 'Common Goods:Cultures Meet Through Craft', which featured crafts made by artists from various Commonwealth countries and 'CARVE:Indigenous carving practices', a series of demonstrations of traditional indigenous carving practices and techniques from Australia, New Zealand and Canada.

Besides that, there was a producers' market, 'Victorian Producers' Market', where the best produces from regional Victoria such as wine, cheese and others were sold. A cooking competition, 'Culinary Pro Am of the Commonwealth' was also held between top Melbourne chefs, each representing a Commonwealth country.

Another crowd drawer was the large screen on museum grounds where live actions of the Games were shown.

The Melbourne Museum was one of Denton Corker Marshall's award-winning projects. One award in particular was the RACV Award for major tourist attraction, where it received 1,428,238 visitors during the years of 2010-11, which the Melbourne Museum received top honours for. In March 2012, the Qantas Australian Tourism Awards will be held in Cairns, where the Melbourne Museum will be represented for Victoria as a national level.[6] Melbourne Museum’s Science and Life gallery was honoured with the Large Permanent Exhibition Award due to its outstanding design and flow, among many other awards during 2010 – 11.[7] Their accomplishments have given them a place in numerous awards, being honoured for their high design quality throughout their international practises. They have received awards from the Royal Australian Institute of Architects (RAIA) that top any other firm, one of which was rated most prestigious and highest honour; of their contributions to Australian architecture.[8]